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Ontogeny of Tetrodotoxin Levels in Blue-ringed Octopuses: Maternal Investment and Apparent Independent Production in Offspring of Hapalochlaena lunulata

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Abstract

Many organisms provision offspring with antipredator chemicals. Adult blue-ringed octopuses (Hapalochlaena spp.) harbor tetrodotoxin (TTX), which may be produced by symbiotic bacteria. Regardless of the ultimate source, we find that females invest TTX into offspring and offspring TTX levels are significantly correlated with female TTX levels. Because diversion of TTX to offspring begins during the earliest stages of egg formation, when females are still actively foraging and looking for mates, females may face an evolutionary tradeoff between provisioning larger stores of TTX in eggs and retaining that TTX for their own defense and offense (venom). Given that total TTX levels appear to increase during development and that female TTX levels correlate with those of offspring, investment may be an active adaptive process. Even after eggs have been laid, TTX levels continue to increase, suggesting that offspring or their symbionts begin producing TTX independently. The maternal investment of TTX in offspring of Hapalochlaena spp. represents a rare examination of chemical defenses, excepting ink, in cephalopods.

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Acknowledgements

David Baxter provided H. fasciata natural history information and assistance collecting in Manly. Collecting permits for H. fasciata were supplied by the New South Wales Fisheries Department, Australia (permit #s P05/0101-1.0 & P05/0101-2.0). Julie Himes provided help with animal care and octopus breeding at the University of California, Berkeley (UCB). Drs. Michael Pfrender, Daryll DeWald, Jon Takemoto, and Paul Wolf at Utah State University (USU) shared equipment and advice. Dr. Daniel Mulcahy at Brigham Young University volunteered for fieldwork and Dr. Christine Huffard at Monterey Bay Research Institute assisted with octopus dissections. We thank Dr. Isao Kubo for discussions on the structure and chemistry of TTX. Stephanie Bush, Joey Pakes, Jean Alupay, and Dr. David Lindberg at UCB, Dr. Christine Huffard at MBARI, and Dr. Christopher Feldman at the University of Nevada, Reno, provided comments on earlier drafts of this manuscript and their aid was appreciated. The Department of Integrative Biology (UCB) and the University of California Museum Of Paleontology funded this project through the Summer Research Grant and Graduate Student Research Grant to BLW. Funding was also provided by NSF grant #DEB-031572 to EDB Jr.

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Authors and Affiliations

  1. Department of Biology, New Mexico State University, MSC 3AF, PO BOX 30001, Las Cruces, NM, 88003-8001, USA

    Becky L. Williams

  2. Hopkins Marine Station, Stanford University, 120 Oceanview Blvd, Pacific Grove, CA, 93950-3024, USA

    Charles T. Hanifin

  3. Department of Biology, Utah State University, 5305 Old Main Hill, Logan, UT, 84322-5305, USA

    Edmund D. Brodie Jr.

  4. Department of Integrative Biology, University of California, Berkeley, 3060 Valley Life Sciences Bldg #3140, Berkeley, CA, 94720-3140, USA

    Roy L. Caldwell

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  1. Becky L. Williams
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Correspondence to Becky L. Williams.

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Williams, B.L., Hanifin, C.T., Brodie, E.D. et al. Ontogeny of Tetrodotoxin Levels in Blue-ringed Octopuses: Maternal Investment and Apparent Independent Production in Offspring of Hapalochlaena lunulata . J Chem Ecol 37, 10–17 (2011). https://doi.org/10.1007/s10886-010-9901-4

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